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Evolution in the Understorey: the Sulawesi Babbler Pellorneum Celebense

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Evolution in the Understorey: the Sulawesi Babbler Pellorneum Celebense Zoologischer Anzeiger 293 (2021) 314e325 Contents lists available at ScienceDirect Zoologischer Anzeiger journal homepage: www.elsevier.com/locate/jcz Evolution in the understorey: The Sulawesi babbler Pellorneum celebense (Passeriformes: Pellorneidae) has diverged rapidly on land- bridge islands in the Wallacean biodiversity hotspot * Fionn O Marcaigh a, , David J. Kelly a, Darren P. O'Connell a, b, c, Daniel Dunleavy a, Alice Clark a, Naomi Lawless a, Adi Karya d, Kangkuso Analuddin d, Nicola M. Marples a a Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, D02 CX56, Ireland b School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, NE1 7RU, UK c School of Biology and Environmental Science, University College Dublin, Dublin, D04 N2E5, Ireland d Department of Biology and Biotechnology, Universitas Halu Oleo, Kendari, South-east Sulawesi, Indonesia article info abstract Article history: Tropical islands hold great treasures of Earth's biodiversity, but these fragile ecosystems may be lost Received 8 March 2021 before their diversity is fully catalogued or the evolutionary processes that birthed it are understood. We Received in revised form ran comparative analyses on the ND2 and ND3 mitochondrial genes of the Sulawesi babbler Pellorneum 5 July 2021 celebense, an understorey bird endemic to Sulawesi and its continental islands, along with its Accepted 7 July 2021 morphology and song. Genetic, acoustic, and morphological data agree on multiple isolated populations, Available online 8 July 2021 likely representing independently evolving lineages. The Sulawesi babbler shows signs of rapid specia- Corresponding editor: Alexander Kupfer tion, with populations diverging between Central and Southeast Sulawesi, and even on land-bridge islands which were connected within the last few tens of thousands of years. The genetic divergence Keywords: between Sulawesi babbler populations in this time has been around 33% of their divergence from sister Cryptic biodiversity species which have been isolated from Sulawesi for millions of years. This is likely facilitated by the Incipient speciation Sulawesi babbler's understorey lifestyle, which inhibits gene flow and promotes speciation. Similar Island biogeography patterns of endemism are seen in Sulawesi's mammals and amphibians. This work highlights the un- Pellorneidae documented biodiversity of a threatened hotspot, wrought by complex processes of speciation which Integrative taxonomy interact with ecology and geology. Subspecific taxonomy has at times been controversial, but we argue Wallacea that discrete populations such as these play a key role in evolution. Lying as they do at the heart of the biodiversity hotspot of Wallacea, these islands can reveal much about the evolution of biodiversity at all of its levels, from the gene to the ecosystem. © 2021 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 1. Introduction Wallace (1880) noted that islands vary in their geographical isola- tion, with important consequences for evolution. Some, which they The 20th century Biological Species Concept cemented the termed oceanic islands, were created by volcanic eruptions or uplift importance of isolation in evolutionary biology, with pivotal works of coral far out at sea. Oceanic islands are separated from continents like those of Mayr (1942, 1959) and Dobzhansky (1937, 1940) and other large landmasses by deep seas, and thus have never been showing that populations become species when they are isolated, connected to them by land. Continental land-bridge islands, on the first geographically and then reproductively. The role of geographic other hand, are formed from parts of the continental shelf, and so at isolation in speciation continues to inspire debate, particularly in times of reduced sea level they were a continuous part of the the evolutionary marvels that are the world's islands (e.g. Flantua mainland. Though later work has elaborated on this original clas- et al., 2020; Itescu et al., 2020). Early biogeographers such as sification (Ali, 2017, 2018), much research on island speciation still focuses on highly isolated oceanic islands such as Hawaii and the Galapagos (Whittaker et al., 2017). A smaller, but growing, body of literature has drawn important evolutionary conclusions from the * Corresponding author. faunas of land-bridge islands (e.g. Lister, 1989; Vartanyan et al., E-mail address: [email protected] (F. O Marcaigh). https://doi.org/10.1016/j.jcz.2021.07.006 0044-5231/© 2021 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). F. O Marcaigh, D.J. Kelly, D.P. O'Connell et al. Zoologischer Anzeiger 293 (2021) 314e325 1993; Keogh et al., 2005; Itescu et al., 2020), which are numerically with an adjoining microcontinent to form Buton (or Butung) Island more numerous, ecologically more complex, and zoologically richer (Satyana & Purwaningsih, 2011). The seas between these five than are oceanic islands (Meiri, 2017). As land-bridge islands have islands are both shallow and narrow, and they were connected by been isolated only briefly, these studies provide evidence of evo- land within the last 20,000 years (Nugraha & Hall, 2018). lution which has taken place at a rapid rate. The diversity of islands and species found in Sulawesi make it an Isolation of an island population results from features of the ideal place to study evolutionary divergence across islands. As well species as well as the island, as some organisms are more likely to as the land-bridge islands described here, there are more isolated maintain gene flow across water barriers than others. Thus, studies islands, including the Sula group and the Wakatobi (or Tukangbesi) of evolution on land-bridge islands tend to focus on particularly archipelago, which have never been connected to Sulawesi by land weak dispersers, such as terrestrial mammals and reptiles (e.g. (Nugraha & Hall, 2018). Descriptions of endemic species from these Lister, 1989; Vartanyan et al., 1993; Keogh et al., 2005). However, more isolated islands indicate that birds readily speciate when even among birds and other strongly dispersing animals, certain separated by such permanent barriers (Kelly et al., 2014; O'Connell ecological and behavioural traits will inhibit gene flow across bar- et al., 2019b; Rheindt et al., 2020). The Sulawesi babbler is found on riers which the organism should be physically capable of crossing all the land-bridge islands of Southeast Sulawesi, making it an ideal (Harris & Reed, 2002). Some birds that fly long distances over land candidate for studies of evolutionary divergence on this shorter will not cross even narrow bodies of water (Diamond, 1981), and time scale. As the populations on Sulawesi, Buton, Kabaena, Muna, even the dispersive species that do colonise remote islands can and Wawonii have been separated for an evolutionarily brief period develop “behavioural flightlessness” in these isolated populations of time, any divergence between them is evidence of evolution (Moyle et al., 2009). The habit of foraging in forest understorey occurring at a rapid pace. These islands remain poorly known seems to be particularly significant in limiting gene flow and ornithologically, with species inventories emerging only recently driving speciation (Burney & Brumfield, 2009; Smith et al., 2014). (Martin et al., 2012; Martin et al., 2015; Martin et al., 2017; This study aims to investigate evolution on the land-bridge islands O'Connell et al., 2017; O'Connell et al., 2019a). As pressures on surrounding Sulawesi using a bird which is limited to the forest Indonesia's birds continue to mount (Rentschlar et al., 2018), it understorey, the endemic Sulawesi babbler Pellorneum celebense. becomes increasingly urgent that we study recently documented This species was first described, as Trichastoma celebense, by populations such as these, in order to estimate their evolutionary Strickland (1849). The genus Trichastoma (Blyth, 1842) was sub- distinctiveness and consider their conservation. sumed into Pellorneum (Swainson, 1831)byMoyle et al. (2012) and The Sulawesi babbler belongs to the family Pellorneidae (ground Cai et al. (2019). Our taxonomy follows Gill et al. (2021). babblers), which was formed after species were split from the Sulawesi is the largest island of the Wallacea region, one of Timaliidae, Sylviidae, and Cisticolidae on molecular evidence (Cai Earth's threatened biodiversity hotspots (Myers et al., 2000). et al., 2019). Babbler systematics are complex, and scientists' in- Sulawesi's complex geology has shaped an “anomalous” biogeog- terpretations of them have changed repeatedly over the years raphy (Wallace, 1880) and a high level of endemism (Stattersfield (Cibois et al., 2002; Cibois, 2003; Gelang et al., 2009; Moyle et al., et al., 1998), with the island divided into four distinct peninsulae 2012; Cai et al., 2019). Pellorneid species richness reflects their or “arms”, here referred to as North, Central, South, and Southeast biogeographic history (Cai et al., 2020), being highest in the Sino- Sulawesi (Fig. 1) (the centre of the island, between the arms, also Himalayan Mountains (where the group originated) and in the forms part of Central Sulawesi). Southeast Sulawesi and the islands Sundaland region. Though Wallacea lies immediately to Sunda- of Kabaena, Muna, and Wawonii (or Wowoni)
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